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The Role of Model Organisms in the History of Mitosis Research

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The Role of Model Organisms in the History of Mitosis Research Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press The Role of Model Organisms in the History of Mitosis Research Mitsuhiro Yanagida Okinawa Institute of Science and Technology Graduate University, Okinawa 904-0495, Japan Correspondence: [email protected] Mitosis is a cell-cycle stage during which condensed chromosomes migrate to the middle of the cell and segregate into two daughter nuclei before cytokinesis (cell division) with the aid of a dynamic mitotic spindle. The history of mitosis research is quite long, commencing well before the discovery of DNA as the repository of genetic information. However, great and rapid progress has been made since the introduction of recombinant DNA technology and discovery of universal cell-cycle control. A large number of conserved eukaryotic genes required for the progression from early to late mitotic stages have been discovered, confirm- ing that DNA replication and mitosis are the two main events in the cell-division cycle. In this article, a historical overview of mitosis is given, emphasizing the importance of diverse model organisms that have been used to solve fundamental questions about mitosis. Onko Chisin—An attempt to discover new truths by checkpoint [SAC]), then metaphase (in which studying the past through scrutiny of the old. the chromosomes are aligned in the middle of cell), anaphase A (in which identical sister chro- matids comprising individual chromosomes LARGE SALAMANDER CHROMOSOMES separate and move toward opposite poles of ENABLED THE FIRST DESCRIPTION the cell), anaphase B (in which the spindle elon- OF MITOSIS gates as the chromosomes approach the poles), itosis means “thread” in Greek. In the and telophase (the terminal phase of mitosis M19th century, pioneering researchers who during which chromosomes decondense, again developed light microscopic techniques dis- becoming invisible with light microscopy, the covered characteristic thread-like structures nuclear membrane reforms, and the spindle dis- in dye-stained cells before cell division. They assembles) before cytokinesis (cell division) named this stage “mitosis,” for the appearance (see Fig. 1 for terminology related to G1,G2, of the threads. The threads are now known to be S, and M phases, and Fig. 2 for a schematic of condensed chromosomes, which first become the progression of mitosis). visible with light microscopy during a mitotic In comparison with the whole-cell-division stage called prophase. This is followed by pro- cycle, mitosis is a brief period during which metaphase (later known to be important as condensed chromosomes are accurately segre- this stage is controlled by the spindle assembly gated into daughter nuclei with the aid of an Editors: Mitsuhiro Yanagida, Anthony A. Hyman, and Jonathon Pines Additional Perspectives on Mitosis available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a015768 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a015768 1 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press M. Yanagida Chromosome Chromosome condensation segregation M Decondensation G2 G1 S Sister chromatid cohesion Chromosome DNA Centromere DNA replication Figure 1. The cell cycle consists of four phases: G1,S,G2, and M. Mitosis (M phase) is a brief period of the cell- division cycle. Blue denotes chromosomal DNA; red, centromere/kinetochore. S phase, which comprises a period of DNA synthesis, is preceded by a gap (G1 means the first gap) in which there is no DNA synthesis. G1 phase is alternatively called the prereplicative phase. S phase is followed by another gap (G2). Again, there is no synthesis of DNA in G2 unless DNA damage must be repaired by replication. G2 phase eventually enters M phase or mitosis, which completes one cell cycle. Morphological and biochemical events occurring in these phases are described. The cell-cycle concept was developed around 1953. The boundary between G2 and M is somewhat ambiguous because the initiation of prophase is difficult to define in some cells. Although the activation of cyclin-dependent kinase 1 (CDK1) protein kinase and two other protein kinases, polo and aurora B, are generally accepted as biochemical markers for the onset of mitosis, it should be noted that mitosis is a morphological (cell structural) event, and a number of visible cell structural mitotic markers have been proposed, such as nuclear membrane disassembly, chromosome condensation, spindle formation, kinetochore microtubule formation, etc. (see Fig. 2). The end of mitosis is also ambiguous. In telophase, chromosomes are fully segregated, but still condensed. Going into the G1 phase occurs after chromosome decondensation, reformation of the nuclear membrane around daughter nuclear chromatin, then followed by cytokinesis. In many cells, such as Physarum or vertebrate skeletal muscle cells, cytokinesis does not occur, producing multinucleate cells. assemblage of pole-to-pole microtubules called research and also the founder of cytogenetics the spindle. In addition, there are short aster (see Fig. 3) (Paweletz 2001). Flemming de- microtubules that radiate from the spindle poles scribed the behavior of chromosomes during toward the cell cortex, and kinetochore micro- mitosis with amazing accuracy in an 1882 col- tubules that join the attachment region of chro- lection entitled, “Cell substance,nucleus and cell mosomes (called sister kinetochores). This is division.” For visualization of chromosomes, normally followed by a postmitotic event, cyto- Flemming used aniline dyes, which bind to kinesis, which generates two daughter cells. chromosomes. The first person to observe mitosis in detail Chromosome, in Greek, means colored was a German biologist, Walther Flemming (“chroma”) body (“soma”). A chromosome is (1843–1905), who is the pioneer of mitosis an organized structure of DNA, protein, and 2 Cite this article as Cold Spring Harb Perspect Biol 2014;6:a015768 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press Model Organisms in the History of Mitosis Research Eukaryotic cells Prophase Centrosome Chromosome Kinetochore Nuclear membrane Prometaphase Pole-to-pole microtubule Astral microtubule Kinetochore microtubule Metaphase Anaphase A Anaphase B Telophase Figure 2. Higher eukaryotic mitosis. In higher eukaryotic prophase, the nuclear membrane begins to degrade on the onset of chromosome condensation. In fungi, such as yeast, the nuclear membrane remains during mitosis. Centrosomes (called “spindle pole bodies” in yeast) are duplicated and begin to form the mitotic spindle. In prometaphase, the full spindle forms and condensed chromosomes are attached to kinetochore microtubules. In metaphase, chromosomes are aligned at the middle. In anaphase A, sister chromatids are pulled toward opposite poles. In anaphase B, spindle extension occurs. Finally, in telophase, the nuclear membrane reforms. RNA, which changes its form dramatically genetic material by Oswald Avery (Avery et al. during the cell cycle and under different phys- 1944). iological and physicochemical conditions. Sig- Flemming used a species of salamander as nificantly, most of Flemming’s work was per- the source of his material because salamanders formed before the rediscovery (1900) of the have very large chromosomes. The genome (a genetic principles discovered by Gregor Mendel haploid, or single set of chromosomes) size may (1822–1884). Flemming had no knowledge of be approximately 10 times larger than that of DNA, which was discovered as the “nuclein” humans, because it contains a large number of substance in 1869 by a Swiss biochemist, Fried- repetitious DNAs. In Flemming’s day, large cells rich Miescher, and much later identified as the containing large chromosomes were an obvious Cite this article as Cold Spring Harb Perspect Biol 2014;6:a015768 3 Downloaded from http://cshperspectives.cshlp.org/ on September 30, 2021 - Published by Cold Spring Harbor Laboratory Press M. Yanagida Figure 3. (A) Walther Flemming (image is part of the public domain and, therefore, is reprinted free from copyright restrictions). (B) Theodor Boveri (image is part of the public domain and, therefore, is reprinted free from copyright restrictions). (C) Barbara McClintock (image courtesy of the Barbara McClintock Papers, American Philosophical Society; copyright holder is unknown). advantage. The large chromosomes of cells such materials. Chromosomes are gene transmitters. as thin epithelial cells of newt lungs have proven Third, there exists a relationship between the to be extremely useful in making high-resolu- location of individual genes on the chromo- tion movies of mitosis (Rieder and Hard 1990). some and frequencies of crossing over affecting Detailed behavior of individual chromosomes them. In addition, by observing aberrant mi- at the SAC (Li et al. 1993), which regulates toses, Boveri (2008) proposed that scrambled prometaphase, was clearly observed by Nomar- chromosomes produced by abnormal mitosis ski-differential interference contrast video mi- might be the cause of carcinogenesis, so that croscopy (Rieder and Alexander 1990). cancer can originate from a single cell that di- vided abnormally. SEA URCHIN EMBRYOS REVEALED RAPID, REPEATED MITOSES MAIZE REVEALED CHROMOSOME PLASTICITY Theodor Boveri (1862–1915), a German biol- ogist, understood
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